Cited by 572Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsNeural and Behavioral Psychology Studies

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Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood

Kelly, A. M. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X., Milham, M. P.·2009·Cerebral Cortex

DOI 10.1093/cercor/bhn117

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Abstract

Human cerebral development is remarkably protracted. Although microstructural processes of neuronal maturation remain accessible only to morphometric post-mortem studies, neuroimaging tools permit the examination of macrostructural aspects of brain development. The analysis of resting-state functional connectivity (FC) offers novel possibilities for the investigation of cerebral development. Using seed-based FC methods, we examined the development of 5 functionally distinct cingulate-based intrinsic connectivity networks (ICNs) in children (n = 14, 10.6 +/- 1.5 years), adolescents (n = 12, 15.4 +/- 1.2) and young adults (n=14, 22.4 +/- 1.2). Children demonstrated a more diffuse pattern of correlation with voxels proximal to the seed region of interest (ROI) ("local FC"), whereas adults exhibited more focal patterns of FC, as well as a greater number of significantly correlated voxels at long distances from the seed ROI. Adolescents exhibited intermediate patterns of FC. Consistent with evidence for different maturational time courses, ICNs associated with social and emotional functions exhibited the greatest developmental effects. Our findings demonstrate the utility of FC for the study of developing functional organization. Moreover, given that ICNs are thought to have an anatomical basis in neuronal connectivity, measures of FC may provide a quantitative index of brain maturation in healthy subjects and those with neurodevelopmental disorders.

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Duval, P. E., Fornari, E., Décaillet, M., Ledoux, J., Beaty, R. E., & Denervaud, S. (2023) · Developmental Science · doi:10.1111/desc.13389 · Cited by 15
Maternal childhood trauma and perinatal distress are related to infants’ focused attention from 6 to 18 months
Tu, H., Skalkidou, A., Lindskog, M., & Gredebäck, G. (2021) · Scientific Reports · doi:10.1038/s41598-021-03568-2 · Cited by 22
Sex differences in brain and behavioral development
Beltz, A. M., Kelly, D. P., & Berenbaum, S. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814411-4.00027-5 · Cited by 21
Pros and Cons of Using the Informed Basis Set to Account for Hemodynamic Response Variability with Developmental Data
Cignetti, F., Salvia, É., Anton, J., Grosbras, M., & Assaiante, C. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00322 · Cited by 17
Increased functional homotopy of the prefrontal cortex is associated with corpus callosum degeneration and working memory decline
Avelar‐Pereira, B., Bäckman, L., Wåhlin, A., Nyberg, L. H., & Salami, A. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.08.008 · Cited by 22
“During development, a decrease in functional homotopy likely re-ﬂ ects functional specialization, which is part of the natural developmental process (Kelly et al., 2009; Supekar et al., 2009).”
Developmental Resting State Functional Connectivity for Clinicians
Hulvershorn, L. A., Cullen, K. R., Francis, M., & Schreiner, M. W. (2014) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-014-0020-3 · Cited by 18
Functional connectome and neuropsychiatric symptom clusters of Alzheimer's disease
Chang, Y., Hsu, J., Huang, S., Hsu, S., Lee, C., & Chang, C. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.04.054 · Cited by 18
Efficacy of Web-Based Collection of Strength-Based Testimonials for Text Message Extension of Youth Suicide Prevention Program: Randomized Controlled Experiment
Thiha, P., Pisani, A. R., Gurditta, K., Cherry, E., Peterson, D. R., Kautz, H., & Wyman, P. A. (2016) · JMIR Public Health and Surveillance · doi:10.2196/publichealth.6207 · Cited by 17
“In addition to normal developmental changes resulting in heightened emotional activation [27-29] and diminished inhibitory control abilities [30], ninth graders face new challenges associated with the transition to high school, including greater responsibility for seeking help, greater emphasis on romantic relationshi…”
Background
Effect of rs1344706 in the ZNF804A gene on the brain network
Chen, X., Zhang, Z., Zhang, Q.-M., Zhao, W., Zhai, J., Chen, M., Du, B., Deng, X., Ji, F., Wang, C., et al. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.12.017 · Cited by 17
Neural correlates of eating disorders: translational potential
McAdams, C. J., & Smith, W. (2015) · Neuroscience and Neuroeconomics · doi:10.2147/nan.s76699 · Cited by 16
“During adolescence and young adulthood, myelination includes connecting the anterior and posterior regions of the brain, a process associated with abstract thinking, executive function, and decisionmaking.(16,17) These processes have been reported to be altered in adults with eating disorders.”
An exploratory study of resting-state functional connectivity of amygdala subregions in posttraumatic stress disorder following trauma in adulthood
Leite, L. L., Esper, N. B., Lopes, J. R. M., Lara, D. R., & Buchweitz, A. (2022) · Scientific Reports · doi:10.1038/s41598-022-13395-8 · Cited by 18
Variations of Resting-State EEG-Based Functional Networks in Brain Maturation From Early Childhood to Adolescence
Chung, Y. G., Jeon, Y., Kim, R. G., Cho, A., Kim, H., Hwang, H. Y., Choi, J., & Kim, K. J. (2022) · Journal of Clinical Neurology · doi:10.3988/jcn.2022.18.5.581 · Cited by 18
Patterns of risk—Using machine learning and structural neuroimaging to identify pedophilic offenders
Popovic, D., Wertz, M., Geisler, C., Kaufmann, J., Lähteenvuo, M., Lieslehto, J., Witzel, J. G., Bogerts, B., Walter, M., Falkai, P., et al. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1001085 · Cited by 17
Developmental changes between ages 13 and 21 years in the extent and magnitude of the BOLD response during decision making
Keulers, E. H. H., Stiers, P. L. J., & Jolles, J. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.08.059 · Cited by 17
“Maturation most likely also takes the form of maturing connectivity, with more effective long range connections being installed in the course of adolescence (Fair et al., 2007, 2008; Kelly et al., 2009).”
Neural Antecedents of Emotional Disorders: A Functional Magnetic Resonance Imaging Study of Subsyndromal Emotional Symptoms in Adolescent Girls
Das, P., Coulston, C. M., Bargh, D. M., Tanious, M., Phan, K. L., Calhoun, V. D., & Malhi, G. S. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.030 · Cited by 16
Visual motherese? Signal‐to‐noise ratios in toddler‐directed television
Wass, S. V., & Smith, T. J. (2014) · Developmental Science · doi:10.1111/desc.12156 · Cited by 15
“We compared toddler-directed and adult-directed TV programmes (TotTV/ATV).”
Method
Maturation of task-induced brain activation and long range functional connectivity in adolescence revealed by multivariate pattern classification
Keulers, E. H. H., Goulas, A., Jolles, J., & Stiers, P. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.079 · Cited by 16
“Also, functional connectivity changes with age mostly take place between spatially remote areas in widespread brain networks, such as anterior cingulate–insular connections in the task related networks and posterior cingulate– ventral medial prefrontal connections in the default mode network (Fair et al., 2007a, 2008;…”
Influential
PRESENCE DE RÉSEAUX DE NEURONES : OÙ EST LE PLAN POUR NE PAS SE PERDRE DANS L’IMMENSITÉ DE CETTE FORÊT?
Fahim, C. (2023) · Cortica · doi:10.26034/cortica.2023.3793 · Cited by 15
The influence of monetary reward on proactive and reactive control in adolescent males
Bowers, M. E., Morales, S., Buzzell, G. A., & Fox, N. A. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.100934 · Cited by 16
“Additionally, connectivity within and between brain networks changes during adolescence (Kelly et al., 2009; Larsen et al., 2018; Supekar et al., 2009).”
Background
Brainnetome atlas of preadolescent children based on anatomical connectivity profiles
Li, W., Fan, L., Shi, W., Lu, Y., Li, J., Luo, N., Wang, H., Chu, C., Ma, L., Song, M., et al. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac415 · Cited by 17
“A functional connectivity study indicated that the functions of the anterior cingulate subregions, which are associated with cognition, undergo considerable changes during childhood and adolescence and that each subregion matures at different times depending on the specific division of functions (Kelly et al. 2009).”
Background
Resting-State Functional MRI and PET Imaging as Noninvasive Tools to Study (Ab)Normal Neurodevelopment in Humans and Rodents
Millevert, C., Vidas-Guscic, N., Vanherp, L., Jonckers, E., Verhoye, M., Staelens, S. G., Bertoglio, D., & Weckhuysen, S. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1043-23.2023 · Cited by 17
Neural Correlates of Feedback Processing in Toddlers
Meyer, M., Harold Bekkering, A., Janssen, D. J. C., de Bruijn, E. R. A., & Hunnius, S. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00560 · Cited by 15
“Throughout childhood and adolescence, developmental changes of emotional processing are associated to rostral and ventral areas of ACC and their functional connectivity (see Kelly et al., 2009, for a review).”
BackgroundMethod
A deep autoencoder with sparse and graph Laplacian regularization for characterizing dynamic functional connectivity during brain development
Qiao, C., Hu, X., Xiao, L., Calhoun, V. D., & Wang, Y. (2021) · Neurocomputing · doi:10.1016/j.neucom.2021.05.003 · Cited by 16
Frequency specific patterns of resting-state networks development from childhood to adolescence: A magnetoencephalography study
Meng, L., & Xiang, J. (2016) · Brain and Development · doi:10.1016/j.braindev.2016.05.004 · Cited by 15
“The long-range connections increased over development to form complete networks like the RSNs in adults [21,22].”
Spatial migration of human reward processing with functional development: Evidence from quantitative meta‐analyses
Yaple, Z. A., Yu, R., & Arsalidou, M. (2020) · Human Brain Mapping · doi:10.1002/hbm.25103 · Cited by 14
“…cingulate foci reported in studies may be explained by cerebral developments at the onset of puberty such as pruning or redundant synaptic connectivity and myelination, which continue to develop into early adulthood (Giedd et al., 1999; Kelly et al., 2008; Rakic, Bourgeois, & GoldmanRakic, 1994).”
Background
Longitudinal Alterations in Prefrontal Resting Brain Connectivity in Non-Treatment-Seeking Young Adults With Cannabis Use Disorder
Camchong, J., Collins, P. F., Becker, M. P., Lim, K. O., & Luciana, M. M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00514 · Cited by 15
“Because we did not hypothesize laterality effects within ACC or NAcc networks (42, 44), and to minimize the number of regions of interest examined, we converged left and right seeds, resulting in five bilateral ACC seeds (17, 19) and one bilateral NAcc seed (27).”
BackgroundMethodInfluential
The effect of mindfulness training on resting-state networks in pre-adolescent children with sub-clinical anxiety related attention impairments
Kennedy, M. F., Mohamed, A. Z., Schwenn, P., Beaudequin, D. A., Shan, Z., Hermens, D. F., & Lagopoulos, J. (2022) · Brain Imaging and Behavior · doi:10.1007/s11682-022-00673-2 · Cited by 22
“Previous studies established that developmental FC changes in children are characterized by weakened short-range FC that strengthens to long-range FC in adulthood (Kelly et al., 2009; Uddin et al., 2010).”
Background
Longitudinal developmental trajectories of functional connectivity reveal regional distribution of distinct age effects in infancy
Liu, J., Chen, H., Cornea, E. A., Gilmore, J. H., & Gao, W. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad288 · Cited by 20
Behavioral activation sensitivity and default mode network-subgenual cingulate cortex connectivity in youth
Iadipaolo, A. S., Marusak, H. A., Sala‐Hamrick, K., Crespo, L. M., Thomason, M. E., & Rabinak, C. A. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.06.039 · Cited by 16
“Prior research suggests that sgACC-DMN rsFC increases from childhood to young adulthood [24,25] and heightened DMN-sgACC rsFC is associated with depressive disorder severity as well increased levels of rumination from adolescence to adulthood [26,27].”
Background
Sparse deep dictionary learning identifies differences of time-varying functional connectivity in brain neuro-developmental study
Qiao, C., Yang, L., Calhoun, V. D., Xu, Z.-B., & Wang, Y. (2020) · Neural Networks · doi:10.1016/j.neunet.2020.12.007 · Cited by 14
Research on Differential Brain Networks before and after WM Training under Different Frequency Band Oscillations
Tian, Y., Zhou, H., Zhang, H., & Li, T. (2021) · Neural Plasticity · doi:10.1155/2021/6628021 · Cited by 14
“suggest that widespread practice of WM tasks may lead to a permanent enhancement of resting-state frontoparietal connections [4].”
Background
Functional connectivity differences in brain networks from childhood to youth
İçer, S. (2019) · International Journal of Imaging Systems and Technology · doi:10.1002/ima.22366 · Cited by 13
“Kolskar et al looked at the age range of (8-22) years in their work with fMRI during rest and task performance, DMN, cingulo-opercular, visual, subcortical components (bilateral putamen, bilateral thalamus, and cerebellum), frontoparietal-related components and sensorimotor network nodes and examined age-related diffe…”
BackgroundMethod
A Deep Dynamic Causal Learning Model to Study Changes in Dynamic Effective Connectivity During Brain Development
Wang, Y., Qiao, C., Qu, G., Calhoun, V. D., Stephen, J. M., Wilson, T. W., & Wang, Y. (2024) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2024.3423803 · Cited by 13
“Youngadultspresentmorefocusedor organizeddECpatterns,butchildrenshowmorediffusedEC patterns[66].”
Exploring Functional Connectivity Networks with Multichannel Brain Array Coils
Anteraper, S. A., Whitfield, S., Keil, B. R., Shannon, S., Gabrieli, J. D. E., & Triantafyllou, C. (2013) · Brain Connectivity · doi:10.1089/brain.2012.0113 · Cited by 13
“There is converging evidence from recent publications that functional connectivity in ACC changes through brain maturation in healthy subjects (Kelly et al., 2009) and also in attention deﬁcit hyperactivity disorder patients (Qiu et al., 2010).”
Overcoming residual interference in mental set switching: Neural correlates and developmental trajectory
Witt, S. T., & Stevens, M. C. G. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.05.007 · Cited by 14
“In parallel, it has also been suggested that the functional network organization of these regions develops from being defined by local, anatomical proximity during childhood to being defined by distributed functional roles in adulthood (Fair et al., 2007, 2008, 2009; Kelly et al., 2009; Power et al., 2010; Supekar et…”
Extracting information from functional connectivity maps via function-on-scalar regression
Reiss, P. T., Mennes, M., Petkova, E., Huang, L., Hoptman, M. J., Biswal, B. B., Colcombe, S. J., Zuo, X., & Milham, M. P. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.01.071 · Cited by 13
“4, and parallel results in the Supplementary material, especially for the PCC seed) may suggest a continuation, from early to mid-adulthood, of the shift toward a more distributed RSFC architecture that occurs from childhood to adulthood (Fair et al., 2007, 2009; Kelly et al., 2009).”
BackgroundInfluentialSelf-citation
Altered functional connectivity in posttraumatic stress disorder with versus without comorbid major depressive disorder: a resting state fMRI study
Kennis, M., Rademaker, A. R., van Rooij, S. J. H., Kahn, R. S., & Geuze, E. (2014) · F1000Research · doi:10.12688/f1000research.2-289.v2 · Cited by 13
“For the subgenual ACC two spherical seeds (left and right, 3.5 mm radius) were created around two seed point coordinates, as previously described by Kelly et al. (2009)26.”
Influential
Hyperactivity of the default mode network in schizophrenia and free energy: A dialogue between Freudian theory of psychosis and neuroscience
The, J. T., Ansermet, J., Magistretti, P. J., & Ansermet, F. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.956831 · Cited by 15
“The parallel between the Freudian ego and the DMN seems also to be supported by studies that demonstrate that the connectivity between the different nodes in the DMN is absent in newborns, and that it is built and matures during development (Fransson et al., 2007; Fair et al., 2008; Kelly et al., 2009).”
Result
The dynamic programming high-order Dynamic Bayesian Networks learning for identifying effective connectivity in human brain from fMRI
Dang, S., Chaudhury, S., Lall, B., & Roy, P. K. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.05.009 · Cited by 11
An explainable autoencoder with multi-paradigm fMRI fusion for identifying differences in dynamic functional connectivity during brain development
Xu, F., Qiao, C., Zhou, H., Calhoun, V. D., Stephen, J. M., Wilson, T. W., & Wang, Y. (2022) · Neural Networks · doi:10.1016/j.neunet.2022.12.007 · Cited by 11
Classification of recurrent major depressive disorder using a residual denoising autoencoder framework: Insights from large-scale multisite fMRI data
Dai, P., Shi, Y. Q., Lu, D., Zhou, Y. S., Luo, J., He, Z., Chen, Z., Zou, B., Tang, H., Huang, Z., et al. (2024) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2024.108114 · Cited by 11
Resting-State fMRI and Developmental Systems Neuroscience
Uddin, L. Q. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00014 · Cited by 10
“Functional connectivity measures derived from rsfMRI have been used to demonstrate age-related changes in the organization of networks across the whole brain (Fair et al., 2009; Supekar et al., 2009) as well as within specific systems (Kelly et al., 2009).”
BackgroundMethodSelf-citation

Authors: Kelly, A. M. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X., & Milham, M. P.
Affiliations: NYU Langone Health (US)
New York University (US)
Humboldt-Universität zu Berlin (DE)
Nathan Kline Institute for Psychiatric Research (US)
ORCID: Uddin, L. Q.
Shehzad, Z.
Gee, D. G.
Reiss, P. T.
Margulies, D. S.
Castellanos, F. X.
Milham, M. P.
Venue: Cerebral Cortex
Publisher: Oxford University Press (OUP)
Published: 2008-07-24
Volume: 19
Issue: 3
Pages: 640-657
ISSN: 1047-3211 (ISSN-L)
1460-2199
DOI: 10.1093/cercor/bhn117
OpenAlex: W2113490642
Cited by: 572
References: 191
Citations by year: 2026: 10 · 2025: 16 · 2024: 17 · 2023: 22 · 2022: 20 · 2021: 34 · 2020: 25 · 2019: 33 · 2018: 37 · 2017: 37 · 2016: 36 · 2015: 37 · 2014: 63 · 2013: 51 · 2012: 43
FWCI: 15.68
Type: journal article
Language: en
Open access: closed
Locations: Cerebral Cortex (publishedVersion)
PubMed (publishedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: anterior cingulate cortex, resting-state functional connectivity, resting-state networks, brain maturation, developmental trajectories, children, adolescents, young adults, seed-based functional connectivity
MeSH terms: Adolescent, Age Factors, Child, Female, Gyrus Cinguli, Humans, Functional Laterality, Male, Nerve Net, Young Adult

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Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood

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